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A Bound Form of Silicon in Glycosaminoglycans And Proc. Nat. Acad. Sci. USA Vol. 70, No. 5, pp. 1608-1612, May 1973 A Bound Form of Silicon in Glycosaminoglycans and Polyuronides (polysaccharide matrix/connective tissue) KLAUS SCHWARZ Laboratory of Experimental Metabolic Diseases, Veterans Administration Hospital, Long Beach, California 90801; and Department of Biological Chemistry, School of Medicine, University of California at Los Angeles, Calif. 90024 Communicated by P. D. Boyer, March 19, 1973 ABSTRACT Silicon was found to be a constituent of notably hyaluronic acid, chondroitin 4-sulfate, dermatan certain glycosaminoglycans and polyuronides, where it sulfate, and heparan sulfate, contain relatively large amounts occurs firmly bound to the polysaccharide matrix. 330-554 ppm of bound Si were detected in purified hyaluronic acid of the element, not as free silicate ions or silicic acid but as a from umbilical cord, chondroitin 4-sulfate, dermatan firmly bound component of the polysaccharide matrix. High sulfate, and heparan sulfate. These amounts correspond to amounts of bound Si were also detected in two polyuronides, 1 atom of Si per 50,000-85,000 molecular weight or 130-280 pectin and alginic acid. Stability tests and enzymatic studies repeating units. 57-191 ppm occur in chondroitin 6-sulfate, evidence for the assumption that the Si is linked heparin, and keratan sulfate-2 from cartilage, while provide hyaluronic acids from vitreous humor and keratan sulfate- covalently to the polysaccharides in question, possibly as an 1 from cornea were Si-free. Large amounts of bound Si are ether (or ester-like) derivative of silicic acid, i.e., a silanolate. also present in pectin (2580 ppm) and alginic acid (451 ppm). The bound Si is not dialyzable, does not react with MATERIALS AND METHODS ammonium molybdate, is not liberated by autoclaving or Eight of the mucopolysaccharides studied were standard 8 M urea, and is stable against weak alkali and acid. Strong alkali and acid hydrolyze the Si-polysaccharide bond. reference samples obtained from Dr. M. B. Mathews, Depart- Free, direct-reacting, dialyzable silicate is obtained. ment of Pediatrics, University of Chicago, Ill. These samples Enzymatic hydrolysis of hyaluronic acid or pectin does not were prepared under a grant from the National Heart Insti- liberate silicic acid, but leads to products of low molecular tute to serve as reference standards for research on connective weight still containing Si in bound form. It is concluded see ref. The that Si is present as a silanolate, i.e., an ether (or ester- tissue polysaccharides. (For details 14.) following like) derivative of silicic acid, and that R1-O-Si-O-R2 materials were analyzed (see Table 1): hyaluronic acid or R1-O--Si-O-Si-O-R2 bridges play a role in the (standard reference sample), from human umbilical cords, structural organization of glycosaminoglycans and poly- molecular weight 230,000; hyaluronic acid, grade 1, from uronides. Thus, Si may function as a biological cross- human umbilical cord, Sigma Chemical Corp.; hyaluronic linking agent and contribute to architecture and resili- ence of connective tissue. acid from bovine-vitreous humor, P. L. Biochemicals, Inc.; chondroitifi 4-sulfate (standard reference sample) from noto- Silicon (Si) is essential for growth and general development cord of rock sturgeon (Acipenser fulvescens) 98% Cu4 sulfated (1). In all-plastic isolators that exclude the element from the disaccharide, molecular weight 12,000; chondroitin 4-sulfate environment (2, 3), growth of rats is reduced by 30-35% from rat costal cartilage, courtesy of Dr. M. B. Mathews; when Si-deficient aminoacid diets are fed, and bone de- chondroitin 6-sulfate (standard reference sample) from human formations develop. Dietary supplements of silicate prevent umbilical cord (15), 80% C-6 sulfated, 10% Ca4 sulfated, and these symptoms. Similar findings have been reported for 10% unsulfated disaccharide, molecular weight 40,000; chicks (4). Si, moreover, is needed in rats for normal pigment chondroitin 6-sulfate from human cartilage, courtesy of Dr. formation in the enamel of incisors (5). M. B. Mathews; chondroitin 6-sulfate from sturgeon cartilage, Even though it has been known for years that Si occurs in courtesy of Dr. M. B. Mathews; dermatan sulfate (standard small, varying amounts in all animals, very little concrete reference sample) from hog mucosal tissue byproducts of evidence exists about its functional significance and bio- heparin isolation, molecular weight 27,000; heparan sulfate chemical behavior (6, 7). In mammals, Si occurs most abun- (standard reference sample) from beef lung byproducts, dantly in connective tissue and related structures. While calcium salt, assumed molecular weight 15,000-17,000; amounts in blood and parenchymal organs are relatively low, heparin (standard reference sample) from hog mucosal tissues, the Si content of skin, cartilage, ligaments, and other tissues anticoagulant activity 180 U.S.P. international units/mg, of mainly mesodermal origin frequently exceeds 100 ,g/g dry molecular weight 11,000; keratan sulfate-1 (standard reference wt (8)*. sample) from bovine-corneal tissue, molecular weight 16,000; In extensive experiments with cartilage and bovine-nasal keratan sulfate-2 (standard reference sample) from human septum we found Si to be strongly bound -to the organic costal cartilage, heterogenous, containing portions of ma- matrix of these tissues. During attempts to identify the bind- terial incompletely substituted by sulfate; pectin (pectinic ing site of Si we discovered that certain glycosaminoglyeans, acid), purified, from citrus fruit, Nutritional Biochemicals Corp., molecular weight 100,000-200,000; alginate from Laminaria digitata, courtesy of Dr. Arne Haug, Institute for * Reported Si amounts vary greatly, depending on the analytical methods used. A large number of results (9, 10) obtained before Marine Biochemistry, Trondheim, Norway, containing of suitable methods (11, 12) and the advent of about 60o D-mannuronic and 40% Laminaria-guluronic acid; development of Dr. plastic laboratory ware are much higher than those found more alginate, prepared from Laminaria digitata, courtesy recently (8, 13). Many of these older data must be discarded. Arne Haug, containing about 40% D-mannuronic acid and 1608 Downloaded by guest on September 26, 2021 Pw.'Nat. Acad. Sci. USA 70 (1973) Bound Si in Glycosaminoglycans and Polyuronides 1609 60% Laminaria-guluronic acid, average molecular weight TABLE 1. Free, total, and bound Si in glycosaminoglycans, 200,000; glycogen, purified, from rabbit liver, Nutritional polyuronides, and some glycans Biochemicals Corp., average molecular weight 1,000,000, total ash 0.13%; starch, purified, from corn, General Bio- Si (p4g/g) chemicals, Inc.; Dextran (Clinical Grade), Nutritional Bio- Bound chemicals Corp., molecular weight 200,000-300,000 (median (total minus 254,000), prepared from culture medium of Leuconostoc Substance and source Free Total free) mesenteroides (NRRL-B512), 1,6-linked with slight trace of 1,3-linked glucoside, ash; inulin, purified, from Dahlia Glycosaminoglycans 0.02% Hyaluronic acid tubers, Sigma. (a) Human umbilical cord 25 354 329 Plastic laboratory ware was used in all procedures, except (b) Human umbilical cord 1533 1892 359 for pH measurements done with a miniature combination (c) Bovine vitreous humor 980 949 glass electrode. Samples were kept covered during practically Chondroitin 4-sulfate all manipulations to avoid Si contamination from dust. (d) Notocord of rock sturgeon 44 598 554 Si was determined by the technique devised by King and (e) Rat costal cartilage 30 361 331 collaborators (11), as modified by McGavac et al. (12, 13). Chondroitin 6-sulfate The method is based on the formation of silicomolybdate (f) Human umbilical cord 45 123 78 (SiO2. 12Mo02) and the production of a blue color upon re- (g) Human cartilage 36 227 191 duction. Interference by phosphate ions was not a problem in (h) Sturgeon cartilage 64 121 57 these ana ses. In addition to colorimetric Si determinations, Dermatan sulfate (i) Hog mucosal tissue 46 548 502 several materials were subjected to emission spectroscopy, by Heparan sulfate Mr. George Alexander and staff, Laboratory of Nuclear (j) Beef lung 39 466 427 Medicine and Radiation Biology, University of California at Heparin Los Angeles. (k) Hog mucosal tissue 33 175 142 In the colorimetric assay, 1 ,ug of Si produced an absorbance Keratan sulfate-1 of 0.167; the detection limit was 0.03 ,g of Si. Complete re- (1) Bovine cornea 31 37 agent blanks were applied side-by-side with the analyzed Keratan sulfate-2 specimen. Whenever samples were subjected to procedures (m) Human costal cartilage 37 105 68 such as dialysis, autoclaving, or hydrolysis, blanks were Polyuronides simultaneously treated in identical fashion. The following Pectin chemicals were used: ammonium molybdate, (NH4)6Mo7024 - - (n) Citrus fruit 5 2586 2581 4H20, sodium sulfite, ferric chloride, sodium acetate, an- Alginic acid hydrous powder (all analyzed reagents); and 1,2,4-amino- (o) Horsetail kelp 43 naphthol-sulfuric acid (all from J. T. Baker Chemical Co.); (p) Horsetail kelp 5 456 451 sulfuric acid, 95-97%, A.C.S. reagent (Dupont); sodium Polyglycans metabisulfite, reagent (Matheson, Coleman & Bell); sodium Glycogen carbonate, anhydrous powder, A.C.S. analytical reagent, and (q) Rabbit liver 8 34 26 hydrochloric acid, analyzed reagent, U.S.P. (Mallinckrodt); Starch congo red, certified (Allied Chemical). (r) Corn - 22 The colorimetric method was used to determine
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